Introduction

The fishery sector in India plays a major role in the country's socio-economy. The black pomfret, Parastromateus niger (Bloch), the only known member of the genus Parastromateus Bleeker (Carangidae), is commercially harvested in India. This pelagic fish species, often occurring in large schools in depths of 15–40 m, generally over muddy bottoms (Yadollahvand and Rahnama 2014; Froese and Pauly 2023; Fricke et al. 2023). It is broadly distributed across the Persian Gulf and the Oman Sea, tropical, subtropical, and temperate seas of the world, the Indian and the Pacific Oceans, China and the Malay Archipelago and most abundant on the west coast of India and Indonesia (Froese and Pauly 2023; Fricke et al. 2023). Information regarding the parasitic infestation of swift-swimming fishes in the open water is scanty. Few reports are available about the parasitic crustaceans infesting P. niger, and the buccal cavity, operculum, gill apparatus and body surface of P. niger are common niches for ectoparasites (Pillai 1985).

The great majority of parasitic crustaceans on marine fish belong to groups such as Copepoda and Isopoda (Margolis et al. 1982; Oktener and Sezgin 2000; Maran et al. 2012). Reports showed that marine fishes are highly susceptible to parasitization with copepods and isopods (Pillai 1985; Helna et al. 2016, 2018, 2023; Aneesh et al. 2021a, b, 2022a, b; Nashad et al. 2022). Many marine fishes are known to host more than one species of parasitic crustaceans (Yamaguti and Yamasu 1959; Ohtsuka et al. 2009; Aneesh et al. 2023a), even though a comprehensive study involving the simultaneous infestation, prevalence, site, and niche specificity of each parasitic species is highly necessary. The present study addressed in detail the ectoparasitic crustacean infestation on P. niger from Indian waters with special reference to the host specificity, site specificity and niche separation of each species recovered. The rate of infestation on host fish in terms of prevalence, mean intensity and mean abundance are discussed in detail. The present study also reviewed and discussed the simultaneous multiple co-occurrence of parasitic crustaceans.

Materials and Methods

A total of 162 fish, P. niger were collected and examined from February 2016 to January 2021 as part of the routine sampling. Collected specimens of Black pomfret P. niger were collected from various fish landing centers from different localities (Fig. 1) along the Kerala coast of the Arabian Sea (Bekal, 12°24′05''N, 75°00′45''E; Azhikkal, 11°56′36"N, 75°18′36"E; Ayyikkara, 11°51′30"N, 75°22′27"E; Perumatura, 8°37′40''N; 76°47′16''E; Ponnani, 10°46′57.9"N, 75°54′32"E), the southwest coast (Muttom, 8°07′48" N, 77°19′12"E); the Chennai Coast in the Bay of Bengal (Marina Beach, 13°02′57"N, 80°16′58"E) and Coromandel Coast. Soon after collection, the fish were thoroughly examined (general body surface, lateral line region, the base of the pectoral fin, near operculum and posterior-ventral sides, branchial cavity, gill filaments, inner wall of operculum, buccal cavity, etc.) for the presence of parasitic crustaceans. Recovered specimens were preserved in 90% ethanol. Methods for preservation, dissection, and mounting for identification were according to the techniques described in Aneesh et al. (2018, 2023b). The identification was performed using a dissection microscope and microphotographed by using multi focusing stereo microscope Leica-M205A, according to Pillai (1985) and Martin et al. 2016. The prevalence (P), mean intensity (I), and mean abundance were calculated according to Margolis et al. (1982) and Bush et al. (1997). Since we depended on fish markets for the study, the actual parasitism may have been underestimated, since during the time of processing, some pre-adult stages of parasitic copepods may have been lost. Sources for the fish taxonomy and host nomenclature were based on Fish Base (Froese and Pauly 2023) and Catalogue of Fishes (Fricke et al. 2023). The body length of the cymothoid is measured from the cephalon to the distal margin of the pleotelson. The total length of the copepods excludes egg strings. Mean and standard deviation are calculated in Excel, and the total number is given (N).

Fig. 1
figure 1

Map illustrating the location of sampling sites of the Black pomfret Parastromateus niger (Carangidae), along the Kerala coast of the Arabian Sea (Bekal, 12°24′05''N, 75°00′45''E; Azhikkal, 11°56′36"N, 75°18′36"E; Ayyikkara, 11°51′30"N, 75°22′27"E; Perumatura, 8°37′40''N; 76°47′16''E; Ponnani, 10°46′57.9"N, 75°54′32"E), the southwest coast (Muttom, 8°07′48" N, 77°19′12"E), and the Chennai Coast in the Bay of Bengal (Marina Beach, 13°02′57"N, 80°16′58"E) (source: https://www.google.co.in/maps)

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Results

A total of 162 P. niger were collected and examined. More than 70% (117 out of 162) of the examined fishes were infested with parasitic crustaceans. Six species of parasitic crustaceans, including one cymothoid isopod, Cymothoa eremita (Brünnich, 1783), and five species of copepods from five different families, i.e. Lernaeenicus stromatei Gnanamuthu 1953 (Pennellidae), Bomolochus megaceros Heller, 1865 (Bomolochidae), Lernanthropus koenigii Steenstrup and Lütken, 1861 (Lernanthropidae), Synestius caliginus Steenstrup and Lütken, 1861. (Caligidae) and Thysanote appendiculata (Steenstrup and Lütken, 1861) (Lernaeopodidae) were found to be using P. niger as a host (Figs. 2, 3, 4 and 5). A total of 357 parasitic copepods, including 148 B. megaceros, 31 S. caliginus, 8 (+ 2 males attached with females) L. koenigii, 41 T. appendiculata, 134 L. stromatei, and 30 individuals of cymothoid C. eremita, were recovered from the infested host fishes (Table 1).

Fig. 2
figure 2

Parasitic crustacean infesting the Black Pomfret, Parastromateus niger (Bloch, 1795). a Parastromateus niger; b Cymothoa eremita (Brünnich, 1783) - female; c Synestius caliginus Steenstrup & Lütken, 1861 - female; d Bomolochus megaceros Heller, 1865 - female; e Thysanote appendiculata (Steenstrup & Lütken, 1861)- female; f Lernanthropus koenigii Steenstrup & Lütken, 1861 - female; g Lernaeenicus stromatei Gnanamuthu, 1953 - female

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Table 1 Parasitological indices of the parasitic crustaceans infesting Parastromateus niger (Bloch) from India
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Systematic account

Order Isopoda Latreille, 1817

Suborder Cymothoida Wägele, 1989

Superfamily Cymothooidea Leach, 1814

Family Cymothoidae Leach, 1814

Genus Cymothoa Fabricius, 1793

Syn. (See Aneesh et al. 2022b).

Cymothoa eremita (Brünnich, 1783)

(Figs. 2b and 3)

Fig. 3
figure 3

Cymothoa eremita (Brünnich, 1783) ovigerous female ex Parastromateus niger (Bloch): a dorsal view; b ventral view; c lateral view; d anterior view of pereonite 1 and cephalon; e dorsal view of pleonites and pleotelson; f ventral view of cephalon

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Syn. (See Martin et al. 2016).

The buccal attaching C. eremita, is a widely known species and it can be identified by the following combinations of characters: 1) anterolateral margins of pereonite 1 extending nearly half the length of cephalon; 2) subtruncate cephalon; 3) small horn-like structures on the posterolateral margins of pereonite 1; 4) pleon as wide as pereon; 5) uropods not extending to pleotelson posterior margin; 6) pereopod 7 with a bulbous protrusion on ischium. It was recovered from the buccal cavity of the black pomfret, Parastromateus niger, over the tongue. Among 162 fish (P. niger) examined, 29 were found to be parasitized with Cymothoa eremita; the prevalence and mean intensity being 17.9% and 1.03, respectively (Table 1). Except for one male, all other recovered parasites (C. eremita) were ovigerous females with or without brood. Females were attached to the floor of the buccal cavity, their cephalon facing towards the opening of the host mouth; the male settled just behind the female on the gill arch.

Size: ovigerous females, 27.87 ± 2.92 mm (N = 29), male 8.00 mm (N = 1).

Colour: ovigerous female and male-tan colour.

Other host records: recorded from P. niger (as Stromateus niger); Psettodes erumei (Bloch and Schneider); Liza vaigiensis (Quoy and Gaimard) (as Mugil waigiensis) and Peprilus paru (Linnaeus) (as Stomateus paru); Psuedanthias evansi (Smith); Arothron leopardus (Day) (as Tetrodon leopardus); Tetrodon sp.; Hime formosana (Lee and Chao) (as Aulopus japonicus); Parastromateus sp. and Psettodes sp.; Pampus argenteus (Euphrasen) (as Stromateus cinereus); Siganus canaliculatus (Park) (as S. oramin); Plectorhinchus nigrus (Cuvier) (as Pseudopristipoma nigrum); Sphyraena obtusata Cuvier (see Martin et al. 2016 for detailed references).

Distribution: Cymothoa eremita is widely distributed in the Indian Ocean and Indo-Pacific, Japan –Pescsdores, the Philippines and Indonesia – the Cape York Peninsula, Australia, and East to the Society island, Singapore, Malaysia and Bangkok, Ceylon, Arabian Gulf, Indian Peninsula from Madras to Bombay, Mauritius, Seychelles and the Red sea; Japan; and Arabian Gulf; South China Sea; and the Philippines, Hawaii; from southwest coast, Kerala coast, Bay of Bengal and Coromandel Coast of West Bengal, India (see Martin et al. 2016).

Subclass Copepoda Milne Edwards, 1840

Order Cyclopoida Burmeister, 1834

Family Bomolochidae Claus, 1875

Genus Bomolochus von Nordmann, 1832

Bomolochus megaceros Heller, 1865

(Figs. 2d and 4a–b)

Fig. 4
figure 4

a–b Bomolochus megaceros Heller, 1865 ex Parastromateus niger (Bloch), a site of attachment; b ovigerous female; c–d Synestius caliginus Steenstrup & Lütken, 1861 ex Parastromateus niger (Bloch), c ovigerous female; d male; e–f Lernanthropus koenigii Steenstrup & Lütken, 1861 ex Parastromateus niger (Bloch), e. ovigerous female; f male; g–h Thysanote appendiculata (Steenstrup & Lütken, 1861) ex Parastromateus niger (Bloch), g non-ovigerous female; h ovigerous female

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Syn. (See Pillai 1985).

The genus Bomolochus consists of 21 valid species, among them five species have been previously reported from India, including B. megaceros (Pillai 1985; Izawa 2020). This species can be recognized by its comparatively large body and by the long slender, nearly straight processes on the antennule. Bomolochus megaceros (Fig. 4b) was recovered from the inner opercular fold of the host fish. Fifty nine host fish out of 162 examined were infested with B. megaceros and a total of 148 females were recovered; the prevalence and intensity being 36.4% and 2.5 respectively (Table 1). Interestingly all the recovered members were found to be reproductively active females possessing egg sacs and/or maturing ovaries. It also exhibited site and niche-specific parasitization infesting the inner side of the operculum (Fig. 4a), as do several other parasitic crustaceans.

Size: female, 2.86 ± 0.12 mm (N = 148).

Colour: white.

Other host records: P. niger, Caranx djedaba (= Alepes djedaba (Forsskål)), Stromatoides sinensis Forster, Caranx sp., Mugil sp., Therapon theraps Cuvier, Megalaspis cordyla (Linnaeus) (see Pillai 1985).

Distribution: from southwest coast, Kerala coast, Bay of Bengal and Coromandel Coast of West Bengal, Bombay Coast, India, Sri Lanka, South China Sea, China, Baluchistan Taiwan (Pillai 1985).

Order Siphonostomatida Burmeister, 1835

Family Caligidae Burmeister, 1835

Genus Synestius Steenstrup and Lütken, 1861

Synestius caliginus Steenstrup and Lütken, 1861

(Figs. 2c and 4c–d)

Syn. (See Pillai 1985).

The genus Synestius is a monotypic genus with S. caliginus Steenstrup and Lütken, 1861 and have previously been reported from India (Pillai 1985). The female S. caliginus can be identified by the following combinations of features: the presence of two pairs of long club-shaped processes on the genital complex; genital segment enlarged and subequal to cephalothorax in size; abdomen long, club-shaped and two-segmented, longer than processes of genital segment. Seventeen out of 162 observed host fish were infested by Synestius caliginus with a total of 30 females and 1 male; the prevalence being 10.5. Synestius caliginus also exhibits the site specific parasitization, collected from the gill mucous and opercular region of the host.

Size: ovigerous female, 4.61 ± 0.08 mm (N = 30); male, 3.60 mm (N = 1).

Colour: female and male are colorless.

Other host records: P. niger, Pampus argenteus (Euphrasen), Stromatoides sinensis (Pillai 1985).

Distribution: Batavia, Java, Malaysia, Sri Lanka, Persian Gulf, China, Taiwan, from southwest coast, Kerala coast, Bay of Bengal and Coromandel coast of West Bengal, India (Steenstrup and Lütken 1861; Pillai 1985; Present study).

Family Lernanthropidae Kabata, 1979

Genus Lernanthropus de Blainville, 1822

Lernanthropus koenigii Steenstrup and Lütken 1861

(Figs. 2f and 4e–f)

Syn. (See Pillai 1985).

To date the genus Lernanthropus de Blainville, 1822 consists of 103 valid species, among them about 26 species have previously been reported from India including Lernanthropus koenigii Steenstrup and Lütken 1861 (Pillai 1985; Boxshall et al. 2020). Lernanthropus koenigii collected from the gill filaments. This species can be identified by the following combinations of characters: cephalothorax nearly as long as wide; antennular lobe half the width of frontal margin; dorsal plate longer but narrower than anterior division of trunk, nearly equal in length and width, postero-medially concave; genital segment large, longer than broad; abdomen partially fused with genital segment; caudal rami only slightly shorter than abdomen. The lowest prevalence (P = 3.7%) among the recovered parasitic crustaceans is shown by L. koenigii; recovered from only six hosts out of 162 fish and 8 females and 2 males were recovered with the intensity being 1.3. All the eight females were reproductively active, evidenced by the presence of growing ovaries and/or egg sacs. The recovered males were found clinging on the posterior part of the female body in a copulatory position, especially attaching to the genital complex of the females using its maxilliped (these males were not included for calculation of prevalence and mean intensity).

Size: female 4.43 ± 0.07 mm (N = 8), male 2.20, 2.30 mm (N = 2).

Colour: in live condition red in colour.

Other host records: Stromateus paru (= Peprilus paru (Linnaeus)) (Pillai 1985).

Distribution: According to Pillai (1985), Tranquebar, India (Madras, Kerala), southwest coast, Kerala coast, Bay of Bengal and Coromandel coast of West Bengal, India (present study).

Family Lernaeopodidae Milne Edwards, 1840

Genus Thysanote Krøyer, 1863

Thysanote appendicSmyulata (Steenstrup and Lütken, 1861)

(Figs. 2e and 4g–h)

Syn. (See Pillai 1985).

According to Walter and Boxshall (2022) 20 valid species of Thysanote have been reported worldwide among them four species have previously been reported from India (Pillai 1985; Piasecki et al. 2008). Thysanote appendiculata can be identified by the presence of two dichotomously branched processes on each maxilla and each hind corner of trunk with two processes. Out of 162 fish, 32 were infested by T. appendiculata. A total of 41 mature/immature females were recovered from 32 infested hosts; the prevalence and intensity being 19.8 and 1.3, respectively (Table 1). It was recovered from the proximal region of the gill rack.

Size: ovigerous female, 5.99 ± 0.52 mm (N = 41).

Colour: colourless/translucent.

Other host records: P. niger is the only reported host.

Distribution: From southwest coast, Kerala coast, Bay of Bengal and Coromandel coast of West Bengal, India (Pillai 1985; Present study).

Family Pennellidae Burmeister, 1835

Genus Lernaeenicus Le Sueur, 1924

Syn. (See Aneesh et al. 2021a).

Lernaeenicus stromatei Gnanamuthu, 1953

(Figs. 2g and 5)

Fig. 5
figure 5

Lernaeenicus stromatei Gnanamuthu 1953 ovigerous female ex Parastromateus niger (Bloch): a sites of infestation (arrow); b head and neck; c trunk with egg sacs; d habitus dorsal

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Syn. (See Aneesh et al. 2018).

So far 32 valid species of Lernaeenicus have been described, worldwide (Walter and Boxshall 2022) among them ten species have been reported from India (Pillai 1985; Raja et al 2016; Aneesh et al. 2018, 2021a). Lernaeenicus stromatei is identified by the following characters such as, 1) body very long and slender, head, anteriorly rounded and fairly dorso-ventrally flattened and slightly longer than broad (Fig. 5b, c), 2) Three posterior horns, one median and two lateral, all sub-similar and apically rounded, 3) Anterior part of neck with indistinct partition on dorsal side, indicating thoracic segments and a three-segmented antennule. As do other pennellids in the present study L. stromatei also penetrate the flesh of the host fish. Among the parasitic crustaceans recovered in the present study, the second highest prevalence is exhibited by Lernaeenicus stromatei (P = 28.4%). A total of 134 copepods were recovered, the intensity being 2. 9 (Table 1) (Fig. 3). L. stromatei also exhibits a niche specific parasitization, occurring near to opercular bone and gill, burrowed into the body, extending outward through gonopore of the host fish.

Size: ovigerous female, 58.64 ± 10.89 mm (N = 134).

Colour: live specimens are translucent with light red in colour.

Other host records: reported only from P. niger (Gnanamuthu 1953; Pillai 1985; Aneesh 2014; Raja, et al. 2016; Aneesh et al. 2018).

Distribution: Chennai (type locality) (Gnanamuthu 1953; Aneesh et al. 2018, present study), Malabar Coast (Aneesh 2014; present study), West Bengal (present study), South east coast (Raja et al. 2016; Aneesh et al. 2018).

Discussion

Parastromateus niger hosts many parasitic copepod species, listed and described by Pillai (1985). In the present study more than 70% (117 out of 162) of P. niger were infested by parasitic crustaceans. Six species of parasitic crustaceans, including one cymothoid C. eremita and five species of copepods from five different families i.e. B. megaceros, S. caliginus, L. koenigii, T. appendiculata and L. stromatei, were found to be parasitizing P. niger. A total 362 parasitic copepods including 148 B. megaceros, 31 S. caliginus, 8 females (+ 2 males attached with females) L. koenigii, 41 T. appendiculata and 134 L. stromatei and 30 individuals of cymothoid isopod, C. eremita, were collected from the infested host fishes (Table 1). Each parasitic crustacean recovered from P. niger exhibit a strict site and niche specificity. Bomolochus megaceros and L. stromatei were found to be the two major copepod parasites of P. niger with prevalences of 36.4% and 28.4% respectively.

Few reports are available on the simultaneous occurrence of multiple parasitism involving exclusively parasitic crustaceans. Daniel and Rama Rao (1967) reported the simultaneous infestation of another flying fish Parexocoetus mento (Valenciennes) by an external attaching cymothoid isopod, Nerocila sp. and a pennellid copepod, Pennella sp. which was embedded into the body of the host fish. Incidence of double parasitism involving the isopod Nerocila phaiopleura Bleeker, 1857 and the copepod Lernaeenicus sprattae (Sowerby, 1806) was reported in anchovy fish Stolephorus commersonii Lacepède, from Indian waters (Rajkumar et al. 2006). Another marine fish (Hemiramphus far (Forsskål)) also showed simultaneously infestation by the isopod Mothocya plagulophora (Haller, 1880) and the copepod Lernaeenicus hemirhamphi Kirtisinghe, 1932 (Gopalakrishnan et al. 2010).

Heavy simultaneous multiple infestation of parasitic crustaceans was also reported in cartilaginous fishes. Hewitt (1979) reported eight species of parasitic copepods infesting an immature female of white shark, Carcharodon carcharias from Pukerua Bay, near Wellington; including seven species of pandarid copepods such as Pandarus satyrus Dana, 1849 (3 females), Nesippus orientalis Heller, 1865 (15 females), Pandarus bicolor Leach, 1816 (5 females), Echthrogaleus coleoptratus (Guérin-Méneville, 1837) (14 females), E. denticulatus Smith S.I., 1873 (3 females), Dinemoura latifolia (Steenstrup and Lütken, 1861) (9 females, and 1 male), and D. producta (Müller O.F., 1785) (17 females, 3 males) and one species from the family Eudactylinidae, Nemesis lamna lamna Risso, 1826 (61 females and 28 males). Similarly, the multiple infestation of a white shark (C. carcharias) by five different species of pandarid copepods, Dinemoura producta, D. latifolia, Eehthrogaleus coleoptratus, Pandarus bicolor, and Achtheinus oblongus Wilson C.B., 1908 was also observed from Morro Bay, California by Benz et al. (2003).

Even though the cymothoids are usually parasitizing a host fish by a single species, the simultaneous infestation of two isopods was also rarely reported. Williams and Bunkley-Williams (1985) shared the incidence of two different co-occurrences from the Caribbean; 1) co-occurrences of the body surface infesting Anilocra abudefdufi Williams and Williams, 1981 and the branchial infesting Kuna insularis (Williams and Williams 1985) parasitising a single individual host of Abudefduf saxatilis (Linnaeus, 1758), and 2) the external attaching Anilocra acanthuri Williams and Williams, 1981 and the gill infesting Agarna cumulus (Haller, 1880) parasitising Acanthurus chirurgus (Bloch, 1787). Two recent reports on co-occurrence of two cymothoid species includes; co-occurrence of the external attaching Anilocra capensis Leech, 1818 and the buccal-infesting Ceratothoa africanae Hadfield, Bruce and Smit, 2014 on the same individual Pachymetopon blochii (Valenciennes, 1830) from South Africa by Welicky and Smit (2018) and the body surface infesting Anilocra grandmaae Aneesh, Hadfield, Smit and Kumar, 2021 and the branchial infesting Agarna malayi Tiwari, 1952, simultaneously parasitizing the same individual of Tenualosa toli (Valenciennes, 1847) from India (see Aneesh et al. 2022a, b).

Different combinations of species involving the simultaneous multiple infestations were also studied in two belonid fishes from the Malabar coast of India: (1) the banded needle fish, Strongylura leiura (Bleeker, 1850) by one cymothoid isopod, Mothocya renardi (Bleeker, 1857) and three copepods such as Lernanthropus tylosuri Richiardi,1880, Caligodes lacinatus Heller, 1868 and Bomolochus bellones Burmeister, 1833 (see Aneesh et al. 2013), and (2) the spot-tail needlefish, Strongylura strongylura (van Hasselt, 1823) by a cymothoid isopod, Cymothoa frontalis Milne Edward, 1840 and four species of copepods such as L. tylosuri C. lacinatus, B. bellones and Dermoergasilus coleus Cressey and Collette, 1970 (Aneesh et al. 2014).

In the present study the majority of infested P. niger (49%; 57 out of 117) harbors only one species of parasitic crustacean, mostly B. megaceros (44 fishes), rarely C. eremita (8 fish) or L. stromatei (8 fish). Remaining 44% of the host fish (P. niger) (51 out of 117) were also found to be parasitized with any of the two parasitic crustacean species at a time in eight different combinations (see Tables 2 and 3). Among them 41% (21 instances out of 51) were in L. stromatei and T. appendiculata combination, another 10 instances L. stromatei and S. caliginus (see Tables 2 and 3). Simultaneous multiple parasitism (more than two species of parasitic crustaceans in a single fish) was seldom in P. niger. Only 5% (6 out of 117) of infested fishes were simultaneously infested by any of the three parasitic copepods (triple parasitism) in 4 different combinations (see Tables 2 and 3). Quadruple parasitism is very rare in P. niger, only 2.5% (3 out of 117) in three different combinations (see Tables 2 and 3). Multiple parasitism may have been cause by the following factors: migratory routes of the host school, breeding, and distribution of infective stages of parasites etc., even though the occurrence of such phenomena seems to be very rare in the present study and it may be due to the site and niche overlap and reducing inter specific competition.

Table 2 Table showing each species in different levels of parasitism. Total number of fishes examined is 162; NFI- Number of fishes infested
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Table 3 Showing the parasites involved in different levels of parasitism
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In conclusion each species recovered exhibited very strict site specific parasitization. Even though six different species of parasitic crustaceans attached to different sites in the host fish (P. niger), the simultaneous multiple parasitization was very rare.